ORIGINAL ARTICLES. Arch G. Mainous III, PhD; Sharleen P. Johnson, MA; Svetlana Chirina, MPH; Richard Baker, MD

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1 ORIGINAL ARTICLES Academic Family Physicians Perception of Genetic Testing and Integration Into Practice: A CERA Study Arch G. Mainous III, PhD; Sharleen P. Johnson, MA; Svetlana Chirina, MPH; Richard Baker, MD BACKGROUND AND OBJECTIVES: Genetic testing for a variety of diseases is becoming more available to primary care physicians, but it is unclear how useful physicians perceive these tests to be. We examined academic family physicians perception of and experiences with clinical genetic testing and direct-to-consumer genetic testing. METHODS: This study is an analysis of a survey conducted as part of the Council of Academic Family Medicine Educational Research Alliance (CERA). Academic family physicians in the United States and Canada were queried about their perception of genetic testing s utility, how frequently patients ask about genetic testing, and the importance of genetic testing in future practice and education of students and residents. RESULTS: The overall survey had a response rate of 45.1% (1,404/3,112). A majority (54.4%) of respondents felt that they were not knowledgeable about available genetic tests. Respondents perceived greater utility of genetic tests for breast cancer (94.9%) and hemochromatosis (74.9%) than for Alzheimer s disease (30.3%), heart disease (25.4%), or diabetes (25.2%). Individuals with greater self-perceived knowledge of genetic tests were more likely to feel that genetic testing would have a significant impact on their future practice (23.1%) than those with less knowledge (13.4%). Respondents had little exposure to direct-toconsumer genetic tests, but a majority felt that they were more likely to cause harm than benefit. CONCLUSIONS: Academic family physicians acknowledge their lack of knowledge about genetic tests. Educational initiatives may be useful in helping them incorporate genetic testing into practice and in teaching these skills to medical students and residents. (Fam Med 2013;45(4): ) Genetic testing allows a person to obtain information about their risk for a variety of diseases. 1,2 Moreover, genetic information is one of the key steps in developing personalized medicine. 3,4 Personalized medicine using genetic information is not currently the standard of care but is proposed by some authors to be a key component in personalized medicine in the future delivery of care. 3 There are current trends to move genetic knowledge from research laboratories into clinical practice, particularly in primary care. 5 Primary care providers need to be genetically literate. 6,7 Current and future practice will necessitate that providers be familiar with what the genome is, how it can be tested, and basic information about genetics, as well as which diseases have reliable risk markers, and limitations and implications of specific risk markers. 8 Some data suggest that primary care providers in Europe feel unprepared to incorporate genetic information into their practice. 5,9 Incorporating genetic testing into the delivery of health care in primary care includes a variety of barriers and challenges. Providers need to understand when and how to test for a genetic condition that a patient may have and how to counsel patients regarding genetic test results in the context of other clinical findings. It is unclear whether this set of knowledge and skills is being developed in future primary care physicians. Clinical genetic testing in adults is at present typically done for a few patients who, as a result of family history or clinical indications, are considered at risk of carrying genetic variations that are linked to a particular disease or disease From the Department of Family Medicine, Medical University of South Carolina, (Dr Mainous, Ms Johnson, and Ms Chirina;) and the Department of Health Sciences, University of Leicester, Leicester, United Kingdom (Dr Baker). FAMILY MEDICINE VOL. 45, NO. 4 APRIL

2 predisposition. On the other hand, genetic tests are available to test for other diseases, such as cardiovascular disease and diabetes, that are not as clearly linked to specific identifiable genes. Direct-to-consumer genetic testing allows the consumer or patient to submit a saliva or blood sample through the mail and then directly access their personal genetic health care information. 1 A variety of genetic testing companies currently provide genetic risk assessments for a relatively low price. The effect of direct-to-consumer genetic testing on the delivery of health care is also relevant in the delivery of primary care, because many people are looking for a more expedient manner of receiving health care information. 1 It is currently unknown how academic family physicians perceive the phenomenon of direct-to-consumer genetic testing. The aims of this study are to elucidate academic family physicians perception of and experiences with clinical genetic testing and direct-toconsumer genetic testing, their selfassessed knowledge about currently available genetic tests, and how important they think genetic testing should be in the curriculum of medical students and residents. Methods This study is an analysis of a survey conducted as part of the Council of Academic Family Medicine Educational Research Alliance (CERA). CERA is a joint initiative of all four major US academic family medicine organizations (Society of Teachers of Family Medicine [STFM], North American Primary Care Research Group [NAPCRG], Association of Departments of Family Medicine [ADFM], and Association of Family Medicine Residency Directors [AFMRD]). The investigators submitted questions for inclusion in the CERA survey. The survey was designed as an omnibus survey incorporating several distinct subprojects focusing on different topic areas. Practicing physician members of STFM, NAP- CRG, and the ADFM were identified for participation. Although these organizations are all headquartered in the United States, there are some members from outside the United States. In particular, NAPCRG has a substantial number of members from Canada, and therefore we included individuals from the United States and Canada in this study. Since some individuals were members of multiple organizations, unique individuals were selected for the sampling frame. There were 3,112 active unique members of these three organizations in the United States and Canada with valid addresses. The study was approved by the American Academy of Family Physicians Institutional Review Board. The survey was conducted between January 2012 and February The potential respondents were surveyed electronically with an initial invitation for participation. The survey was conducted through the infrastructure of STFM. The survey included a personalized greeting, a letter signed by the presidents of each of the four participating organizations urging participation, and a link to the survey. Nonrespondents were sent up to three follow-up s encouraging participation. Because the survey was structured as an omnibus survey, with several subprojects contained within the overall survey, it was possible for respondents to skip questions. We restricted this analysis to individuals who answered the questions on genetics (n=1,311). The survey questions for this study were developed following a review of the literature to identify key concepts and issues suggesting the need for additional knowledge. The questions are featured at stfm.org/initiatives/cera.cfm. Variables Genetic Testing Practice Behaviors. We assessed current use of and future impact of genetic testing on primary care practice. Respondents were queried regarding their assessment of how often patients ask whether they should receive genetic tests as part of their primary care. The respondents were also asked to estimate the impact genetic testing will have on their clinical practice in the next 5 10 years. Assessment of Value of Genetic Testing in Primary Care. We attempted to evaluate academic family physicians beliefs in the value of genetic testing in primary care. First, respondents were asked to estimate how knowledgeable they feel about currently available genetic tests that they could use in practice. Respondents were asked to provide their estimate of how valuable genetic testing is in primary care for the purpose of determining a patient s risk for disease in comparison to other tools such as physicals, family history, and laboratory tests. Respondents were also asked to estimate the utility of current genetic testing capabilities in determining a patient s risk for several diseases. These included a disease with relatively accepted genetic loci (hemochromatosis), a disease for which genetic risk markers have received significant attention (breast cancer) and diseases for which genetic tests are much less accepted for accurate risk identification (heart disease, diabetes, Alzheimer s disease). Respondents were also asked, In general, how valuable do you feel genetic testing in primary care is for the purpose of determining a patient s best match for treatment? (This is sometimes called personalized medicine.) Direct-to-Consumer Genetic Testing. In an effort to assess the impact of direct-to-consumer genetic tests on primary care practice, two questions were asked about these types of tests. First, the respondents were asked about how often patients ask the physician s advice regarding whether they should take part in direct-to-consumer genetic 258 APRIL 2013 VOL. 45, NO. 4 FAMILY MEDICINE

3 testing. Second, we assessed whether the physician felt that direct-to-consumer genetic testing is more likely to help or harm a patient s general health decisions. Importance of Genetic Testing in Curriculum of Trainees. Consistent with the aim to evaluate how much emphasis academic family physicians feel should be placed on integrating genetic testing into training, we asked the respondents to provide their assessment on how important genetic testing should be in the curriculum of medical students for the purpose of preparing them for primary care practice. We also asked the respondents to provide their assessment on how important genetic testing should be in the curriculum of residents/registrars. Demographics. Respondent demographics of gender, age, and race/ ethnicity were collected, as well as country of practice and proportion of time in clinical practice. Respondent age was assessed by the question, What was your age on your last birthday? The respondent was asked to choose from the following categories (<30 years old, 30 39, 40 49, 50 59, >60 years old). In terms of clinical practice, the respondent was asked On average, how many half days each week do you spend in clinic seeing patients? The respondent selected their practice activity from the response categories of <3 half days, 3 6 half days, or >7 half days. Analysis We first evaluated the data through descriptive statistics. We subsequently examined the relationship between attitudes and demographics using chi-square analysis. Specifically, age and self-assessed knowledge about genetic tests used in primary care were evaluated in relation to attitudes. We focused on self-assessed knowledge as a potentially important variable because of the relevance of knowledge and exposure to new technology and attitudes toward new technology. Results The response rate for the overall survey was 45.1% (1,404/3,112). The characteristics of the respondents are featured in Table 1 and indicate, as expected, that the vast majority of the respondents were from the United States, most (92%) were in clinical care 6 half days per week or less, and two thirds (66.6%) were between 40 and 59 years of age. The respondents did not feel particularly knowledgeable about available genetic tests that they could use in practice. Specifically, a majority (54.4%) felt that they were not knowledgeable about available genetic tests, and 42.9% reported feeling somewhat knowledgeable. When asked to assess, in general, the value of genetic testing for the purpose of determining a patient s risk for disease in primary care in comparison to other tools such as physicals, family history, and laboratory tests, 71.8% felt that it was somewhat or very valuable. The respondents felt that there was less value in genetic testing in primary care for the purpose of determining a patient s best match for treatment, with only 56.0% reporting that it was somewhat or very valuable. The respondents did feel that genetic testing will have a substantial impact on their clinical practice in the next 5 10 years. Only 22.1% felt that genetic testing would have little impact on their future practice. Even fewer felt that genetic testing was not important in the curricula to train medical students (12.8%) and residents (11.3%) for future primary care practice. Table 2 presents the relationship between attitudes toward the value of genetic testing and the respondents self-reported knowledge about available genetic tests. Individuals who have a greater self-perception of knowledge of genetic tests were more likely to predict a greater impact of genetics on clinical practice in the future. A similar relationship was Table 1: Demographic Characteristics of the Respondents Response Sample size (n) 1,311 Male 55.0% Age <40 years old 19.5% years old 29.8% years old 36.8% 60 years old 14.0% Race/ethnicity Non-Hispanic white 82.7% Non-Hispanic Black 3.7% Hispanic 4.3% Asian 6.9% Other/more than one race/declined 2.5% Time spent seeing patients in clinic per week <3 half days 45.1% 3 6 half days 47.1% 7 half-days 7.8% Country of residence United States 97.9% Canada 2.1% FAMILY MEDICINE VOL. 45, NO. 4 APRIL

4 Table 2: Clinical Practice and Attitudes Toward Genetic Testing by Self- Assessed Knowledge of Genetic Tests Used in Primary Care Not Knowledgeable Somewhat or Very Knowledgeable Sample size (n) In general, how valuable do you feel genetic testing in primary care is for the purpose of determining a patient s risk for disease in comparison to other tools such as physicals, family history, and laboratory tests?, % Not valuable in primary care Somewhat valuable in primary care Very valuable in primary care In general, how valuable do you feel genetic testing in primary care is for the purpose of determining a patient s best match for treatment?, % Not valuable in primary care Somewhat valuable in primary care Very valuable in primary care How much of an impact do you think genetic testing will have on your clinical practice in the next 5 10 years?, % Very little Some A significant amount How important do you think genetic testing should be in the curriculum of medical students for the purpose of preparing them for primary care practice?, % Not important Somewhat important Very important How important do you think genetic testing should be in the curriculum of residents/registrars for the purpose of preparing them for primary care practice?, % Not important Somewhat important Very important P Value <.001 <.01 <.001 found with individuals with greater self-perceived knowledge of genetic tests placing greater importance on integrating genetic testing into the curriculum of medical students and residents. Table 3 examines the relationship between beliefs regarding the utility of genetic testing for specific diseases in primary care by self-perceived knowledge of genetic testing. The aggregate responses show that respondents consider genetic tests for breast cancer (94.9%) and hemochromatosis (74.9%) to be somewhat or very useful in determining patient risk for disease. The respondents did not have much confidence in genetic tests for heart disease, diabetes, or Alzheimer s disease, with 69.0% or more responding that current genetic tests were not useful for any of those three diseases. Self-perceived knowledge of genetic testing was not significantly associated with responses on the utility of genetic tests for any of the five queried diseases. Age was significantly associated with perceived utility of genetic tests for two of the diseases (breast cancer and hemochromatosis). For breast cancer, there was not a continuous trend across age groups. For hemochromatosis, younger respondents were somewhat less positive about the utility of genetic tests for this disease (67.5% of respondents <40 years old considered genetic testing to be somewhat or very useful 260 APRIL 2013 VOL. 45, NO. 4 FAMILY MEDICINE

5 Table 3: Relationship Between Perceived Utility of Current Genetic Testing Capability in Determining Patient Risk by Self-Perceived Knowledge of Genetics Not Useful Somewhat or Very Useful Heart disease, overall response, % Heart disease, by self-assessed knowledge, %.83 Not knowledgeable Somewhat or very knowledgeable Breast cancer, overall response, % Breast cancer, by self-assessed knowledge %.40 Not knowledgeable Somewhat or very knowledgeable Diabetes, overall response, % Diabetes, by self-assessed knowledge %.39 Not knowledgeable Somewhat or very knowledgeable Hemochromatosis, overall response, % Hemochromatosis, by self-assessed knowledge, %.51 Not knowledgeable Somewhat or very knowledgeable Alzheimer s disease, overall response, % Alzheimer s disease, by self-assessed knowledge, %.26 Not knowledgeable Somewhat or very knowledgeable P Value compared to 77.3% of respondents 50 years old). In terms of frequency of encounters with patients who ask about direct-to-consumer genetic testing, 70.5% of the respondents replied never, and an additional 27.9% replied rarely, indicating a low frequency of encounters. When asked if direct-to-consumer genetic testing is more likely to help or harm a patient s general health decisions, the majority of respondents (58.1%) agreed that it was more likely to harm, while 10.3% felt it was more likely to help, and 31.6% felt that it was unlikely to make a difference. Discussion This study of academic family physicians shows that a majority of the respondents are not confident in their knowledge about genetic testing in primary care, although they anticipate that genetic testing will have an impact on clinical practice in the future, and most agree that genetic testing is already of some value in determining the risk of some diseases. Further, many felt that education regarding genetic testing for medical students and residents is important. The implications that follow these findings include the need for continued educational opportunities to keep health care providers, especially primary care providers, up to date with currently available genetic tests. Also, primary care providers should be educated about new developments in research in regards to genetic tests so they can differentiate between tests that already show a strong link to the disease from ones that are only theorized. This study also indicates that genetic testing education needs to be improved by either being a larger part of the curriculum in medical school and residency or by using different techniques to improve the learners knowledge base thereby establishing the appropriate background for the rising health care providers. The results suggest that respondents were not enthused about the utility of direct-to-consumer genetic tests, yet they had had little contact with it. Most physicians are comfortable with ordering genetic tests that they feel are indicated. It is possible that more contact with patients bringing in genetic test results may frustrate providers because of the self-directed nature of the patient acquiring genetic tests and the lack of indication for the tests. Counseling of patients regardless of positive or negative results in the context of FAMILY MEDICINE VOL. 45, NO. 4 APRIL

6 unhealthy lifestyle characteristics may still be necessary. The need among primary care physicians for education about genetic testing has been recognized for more than a decade, 10,11 and as the field of genetic testing has continued to advance, the need to deliver the required education is becoming more urgent. The current clinical utility of these findings or impact of not being highly aware of advances in genetic testing is unclear at this point due to the rapid increase in available tests and less than optimal predictive ability of genetic tests for certain common conditions. It should be noted that self-perceived knowledge of genetic testing was not significantly related to determinations of perceived utility of genetic tests for specific diseases. It may be that individuals who are more aware of the predictive capability of current tests are more skeptical of their utility in primary care, particularly in comparison to currently used laboratory tests and history and physical examination. However, because of the expectation of the increased impact of genetic testing on clinical practice in the near future, primary care providers must develop the expertise in genetic testing and counseling. 11 Future research should concentrate on the development and evaluation of interventions to educate primary care physicians and to involve them in new service designs that enable patients to access well-informed services. 12 There are examples of interventions 13 and education programs, 14 and it is now necessary to build on these to establish effective approaches among primary care providers in the United States. Although the results allow us to draw certain important conclusions, there are some limitations associated with the study. The data is based on self-reported indicators that are also based on self-perception rather than a more standardized survey that could be evaluated to provide more conclusive results. Further, the study only includes academic family physicians; however, this group should be particularly up to date as teachers of the next generation of primary care physicians. We investigated comparing the respondents to the nonrespondents within this survey based on the data for which CERA has access. Upon examination of the amount and type of data available in the CERA membership files, we concluded that the available data would not allow us to conduct meaningful analyses regarding differences between respondents and nonrespondents. This was due to the large amount of missing data on demographic variables in the membership database. Nevertheless, in addition to studies of educational interventions, further studies should be considered as a general surveillance tool to detect knowledge deficits related to advances in genetic testing and biomarkers for primary care providers. These types of studies can help update medical school and residency curricula, as well as continuing medical education opportunities, to keep pace with new developments. In conclusion, genetic tests are becoming an important tool in diagnosis and designing treatment. Academic family physicians acknowledge their lack of awareness of genetic testing tools available for the purpose of diagnosis and treatment. Educational initiatives are warranted to address this lacuna and help them to incorporate genetic testing into their practice and provide instruction to medical students and residents. ACKNOWLEDGMENTS: This study was funded in part by cooperative agreement 1U01DD from the Centers for Disease Control and Prevention. We would like to thank Mary Theobald and Jason Pratt for all of their help with CERA. CORRESPONDING AUTHOR: Address correspondence to Dr Mainous, Medical University of South Carolina, Department of Family Medicine, 295 Calhoun Street, Charleston, SC Fax: mainouag@musc.edu. References 1. Bloss CS, Schork NJ, Topol EJ. Effect of directto-consumer genomewide profiling to assess disease risk. N Engl J Med 2011;364: Ormond KE, Wheeler MT, Hudgins L, et al. Challenges in the application of whole-genome sequencing. Lancet 2010;375: Samani NJ, Tomaszewski M, Schunkert H. The personal genome the future of personalized medicine? Lancet 2010;375: Ashley EA, Butte AJ, Wheeler MT, e al. Clinical assessment incorporating a personal genome. Lancet 2010;375: Nippert I, Harris HJ, Julian-Reynier C, et al. Confidence of primary care physicians in their ability to carry out basic medical genetic tasks a European survey in five countries Part 1. J Community Genet 2011;2(1): Emery J, Hayflick S. The challenge of integrating genetic medicine into primary care. BMJ 2001;322: Houwink EJ, van Luijk SJ, Henneman L, van der Vleuten C, Jan Dinant G, Cornel MC. Genetic educational needs and the role of genetics in primary care: a focus group study with multiple perspectives. BMC Fam Pract 2011;12:5. 8. Bellcross CA, Kolor K, Goddard KA, Coates RJ, Reyes M, Khoury MJ. Awareness and utilization of BRCA 1/2 testing among US primary care physicians. Am J Prev Med 2011;40(1): McCahon D, Holder R, Metcalfe A, et al. General practitioners attitudes to assessment of genetic risk of common disorders in routine primary care. Clin Genet 2009;76(6): Escher M, Sappino A-P. Primary care physicians knowledge and attitudes towards genetic testing for breast-ovarian cancer predisposition. Ann Oncol 2000;11: Burke W. Genetic testing in primary care. Annu Rev Genomics Hum Genet 2004;5: Elwyn G, Edwards A, Iredale R, Davies P, Gray J. Identifying future models for delivering genetic services: a nominal group study in primary care. BMC Fam Pract 2005;6(1): Westwood G, Pickering R, Latter S, et al. A primary care specialist genetics service: a cluster-randomised factorial trial. Br J Gen Pract 2012;62(596):e Royal College of General Practitioners. Genetics in primary care. Curriculum Statement 6. London: Royal College of General Practitioners, APRIL 2013 VOL. 45, NO. 4 FAMILY MEDICINE

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